4.7 Article

A hyperactive transcriptional state marks genome reactivation at the mitosis-G1 transition

Journal

GENES & DEVELOPMENT
Volume 30, Issue 12, Pages 1423-1439

Publisher

COLD SPRING HARBOR LAB PRESS, PUBLICATIONS DEPT
DOI: 10.1101/gad.280859.116

Keywords

chromatin; epigenetics; mitosis; transcription

Funding

  1. National Institutes of Health [T32GM008216, R33 1R33EB019767, R56-DK065806, 1U01HL129998, 1RO1 HL119479]
  2. National Institutes of Health New Innovator Award [1DP2OD008514]
  3. Div Of Molecular and Cellular Bioscience
  4. Direct For Biological Sciences [1350601] Funding Source: National Science Foundation

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During mitosis, RNA polymerase II (Pol II) and many transcription factors dissociate from chromatin, and transcription ceases globally. Transcription is known to restart in bulk by telophase, but whether de novo transcription at the mitosis-G1 transition is in any way distinct from later in interphase remains unknown. We tracked Pol II occupancy genome-wide in mammalian cells progressing from mitosis through late G1. Unexpectedly, during the earliest rounds of transcription at the mitosis-G1 transition, similar to 50% of active genes and distal enhancers exhibit a spike in transcription, exceeding levels observed later in G1 phase. Enhancer-promoter chromatin contacts are depleted during mitosis and restored rapidly upon G1 entry but do not spike. Of the chromatin-associated features examined, histone H3 Lys27 acetylation levels at individual loci in mitosis best predict the mitosis-G1 transcriptional spike. Single-molecule RNA imaging supports that the mitosis-G1 transcriptional spike can constitute the maximum transcriptional activity per DNA copy throughout the cell division cycle. The transcriptional spike occurs heterogeneously and propagates to cell-to-cell differences in mature mRNA expression. Our results raise the possibility that passage through the mitosis-G1 transition might predispose cells to diverge in gene expression states.

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